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Computational Identification of Terpene Synthase Genes and Their University of Tennessee, Knoxville TRACE: Tennessee Research and Creative Exchange Doctoral Dissertations Graduate School 5-2016 Computational Identification of erpeneT Synthase Genes and Their Evolutionary Analysis Qidong Jia University of Tennessee - Knoxville, [email protected] Follow this and additional works at: https://trace.tennessee.edu/utk_graddiss Part of the Bioinformatics Commons, Computational Biology Commons, Evolution Commons, Genomics Commons, Plant Biology Commons, and the Systems Biology Commons Recommended Citation Jia, Qidong, "Computational Identification of erpeneT Synthase Genes and Their Evolutionary Analysis. " PhD diss., University of Tennessee, 2016. https://trace.tennessee.edu/utk_graddiss/3654 This Dissertation is brought to you for free and open access by the Graduate School at TRACE: Tennessee Research and Creative Exchange. It has been accepted for inclusion in Doctoral Dissertations by an authorized administrator of TRACE: Tennessee Research and Creative Exchange. For more information, please contact [email protected]. To the Graduate Council: I am submitting herewith a dissertation written by Qidong Jia entitled "Computational Identification of erpeneT Synthase Genes and Their Evolutionary Analysis." I have examined the final electronic copy of this dissertation for form and content and recommend that it be accepted in partial fulfillment of the equirr ements for the degree of Doctor of Philosophy, with a major in Life Sciences. Feng Chen, Major Professor We have read this dissertation and recommend its acceptance: Brian C. O’Meara, Gerald A. Tuskan, Xiaohan Yang Accepted for the Council: Carolyn R. Hodges Vice Provost and Dean of the Graduate School (Original signatures are on file with official studentecor r ds.) Computational Identication of Terpene Synthase Genes and Their Evolutionary Analysis A Dissertation Presented for the Doctor of Philosophy Degree The University of Tennessee, Knoxville Qidong Jia May 2016 © by Qidong Jia, 2016 All Rights Reserved. ii dedicated to my beloved family iii Acknowledgements First, I would like to thank my advisor Dr. Feng Chen for his consistent support, guidance and condence in me during my dissertation work. He is a person with great passion and I sincerely appreciate his help in developing my scientic attitude. I also sincerely appreciate Dr. Albrecht Von Arnim for his tremendous mentorship, encouragement and support. I would also like to express my sincere gratitude to my statistics advisor Dr. Robert Mee for his detailed guidance and advice. Second, I’m very grateful to my committee members, Dr. Brian C. O’Meara, Dr. Gerald A. Tuskan and Dr. Xiaohan Yang for their time, guidance and expertise throughout my dissertation. Finally, and most importantly, my upmost gratitude goes to my parents, parents-in- law and my wife, none of this would have been possible without their unconditional support, sacrice, love and faith in me. iv Abstract Terpenoids, the largest and most structurally and functionally diverse class of natural compounds on earth, are mostly synthesized by plants to be involved in various plant- environment interactions. Some terpenoids are classied as primary metabolites essential for plant growth and development. Terpene synthases (TPSs), the key enzymes for ter- penoid biosynthesis, are the major determinant of the tremendous diversity of terpenoid carbon skeletons. The TPS genes represent a mid-size family of about 30-100 functional genes in almost all major sequenced plant genomes. TPSs are also found in fungi and bacteria, but microbial TPS genes share low levels of sequence similarity and dierent patterns of gene structure with their plant counterparts. Although one common ancestor theory has been suggested and supported by studies from model species, the evolution of plant terpene synthase genes and the evolutionary relationships among terpene synthase genes in plants, bacteria and fungi are still unclear. The recent discovery of microbial- type TPS genes in Selaginella muellendori makes it even more confusing. The goal of this dissertation project is to study the mechanisms that govern the dynamic evolution of terpene synthase genes using comparative genomics methods. Here, we carried out v a large-scale screen to identify terpene synthases in plants (transcriptomes for over 1000 plant species sequenced by the OneKP project and selected genomes from non- seed plants), fungi and bacteria species (sequenced genomes in JGI). Several important discoveries were made by analyzing the data: (1) the microbial-type TPS genes are widely and specically distributed in non-seed land plants; (2) HGT from bacterial to fungi in TPS gene family is identied; (3) a new subfamily x is identied and new insights into the subfamily classication of TPSs are reported by including TPSs identied from large-scale non-seed plant species; (4) the distribution and genomic organization of four types of TPSs in fungi are characterized. These important ndings will help us better understand the evolution of plant secondary metabolism, especially for basal land plants. vi Table of Contents 1 Introduction and Literature Review1 1.1 Terpenoids - Natural Functions and Industrial Uses.............2 1.2 Biosynthesis of Terpenoids...........................3 1.3 Terpene Synthases................................6 1.4 Origin and Evolution of Terpene Synthase Genes..............8 1.5 Objectives.................................... 10 1.6 Bibliography................................... 11 1.7 Appendix..................................... 16 2 Evolution of Typical Plant Terpene Synthase Genes in Non-Seed Plants 19 2.1 Abstract..................................... 20 2.2 Introduction................................... 21 2.3 Results and Discussion............................. 23 2.3.1 Identication of Terpene Synthase Genes from Genomes of Horn- wort, Moss, Liverwort and Two Ferns................ 23 vii 2.3.2 Identication of Terpene Synthases from Non-Seed Plants Tran- scriptomes................................ 24 2.3.3 Search for Terpene Synthase Genes in Green Algae......... 24 2.3.4 Phylogenetic Analysis of TPSs from Non-Seed Plants with TPSs from Selected Seed Plants....................... 25 2.4 Conclusions................................... 28 2.5 Materials and Methods............................. 30 2.5.1 Data Retrieval, Management and Taxonomy Classication..... 30 2.5.2 Identication of Typical Plant Terpene Synthases from Transcrip- tomes of 324 Non-Seed Plants..................... 31 2.5.3 Assembly of Hornwort Anthoceros punctatus Genome and Identi- cation of Terpene Synthases..................... 31 2.5.4 Identication of Terpene Synthases from Marchantia polymorpha and Sphagnum fallax .......................... 32 2.5.5 Identication of Terpene Synthases from Salvinia cucullata and Azolla superorganism .......................... 33 2.5.6 Identication of Terpene Synthases from Lygodium japonicum ... 33 2.5.7 Search for Terpene Synthase Genes in Twelve Algal Genomes and Transcriptomes............................. 34 2.5.8 TPSs on JBrowse............................ 34 2.5.9 Phylogenetic Analyses of Terpene Synthases............ 34 2.6 Bibliography................................... 36 viii 2.7 Appendix..................................... 42 3 Microbial Type Terpene Synthase Genes Occur Widely and Specically in Non-seed Land Plants 60 3.1 Abstract..................................... 62 3.2 Introduction................................... 63 3.3 Results and Discussion............................. 65 3.3.1 Terpene Synthase Genes of Microbial Type are Highly Enriched in the Transcriptomes of Non-Seed Land Plants........... 65 3.3.2 The Majority of MTPSL Genes Identied from Plant Transcrip- tomes Forms Four Groups Clustered with Either Fungal or Bac- terial Terpene Synthases........................ 66 3.3.3 The Majority of MTPSL Genes Identied from Plant Transcrip- tomes are Plant Genes......................... 67 3.3.4 Evolutionary Implications of Non-Seed Plant-Specic MTPSLs.. 71 3.3.5 Biochemical Function of Selected MTPSLs: Diversity of Activities. 74 3.4 Conclusions................................... 75 3.5 Materials and Methods............................. 76 3.5.1 Identication of Terpene Synthases of Microbial Type from Tran- scriptomes and Sequenced Genomes................. 76 3.5.2 Assembly of Hornwort Anthoceros punctatus Genome and Identi- cation of MTPSL Genes........................ 78 ix 3.5.3 Phylogenetic Analyses of Terpene Synthases............ 78 3.5.4 Plant Material, Genomic DNA Isolation and PCR.......... 79 3.6 Acknowledgements............................... 80 3.7 Bibliography................................... 81 3.8 Appendix..................................... 88 4 Horizontal Gene Transfer of Terpene Synthase Genes from Bacteria to Fungi 103 4.1 Abstract..................................... 105 4.2 Introduction................................... 106 4.3 Results...................................... 109 4.3.1 Analysis of Bacterial and Fungal Terpene Synthase Genes Sug- gests Possible HGT Events from Bacteria to Fungi.......... 109 4.3.2 The Apparent Orthologs of BTPSL were Identied in a Group of Entomopathogenic Fungi....................... 110 4.3.3 Collinearity for the Genome Region Containing the BTPSL and the Identication of Neighbor Genes................. 112 4.3.4 Experimental Verication of BTPSL from M. Robertsii as a Fungal Gene................................... 114 4.3.5 The Presence of Typical Fungal TPS Genes in Relevant Fungal Species.................................
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